A host of cellular processes enable plants to defend themselves from disease caused by pathogenic agents. These processes apparently form an integrated set of resistance mechanisms that is activated by initial infection and then limits further spread of the invading pathogenic microorganism.
Subsequent to recognition of a potentially pathogenic microbe, plants can activate an array of biochemical responses. Generally, the plant responds by inducing several local responses in the cells immediately surrounding the infection site. The most common resistance response observed in both nonhost and race-specific interactions is termed the "hypersensitive response" (HR). In the hypersensitive response, cells contacted by the pathogen, and often immediately adjacent cells, rapidly collapse and dry in a necrotic fleck. Other responses include the deposition of callose, the physical thickening of cell walls by lignification, and the synthesis of various antibiotic small molecules and proteins. Genetic factors in both the host and the pathogen determine the specificity of these local responses, which can be very effective in limiting the spread of infection to localized lesions.
The hypersensitive response in many plant-pathogen interactions results from the expression of a resistance (R) gene in the plant and a corresponding avirulence (avr) gene in the pathogen. The resistance gene in the plant and the avirulence gene in the pathogen often conform to a gene-for-gene relationship. That is, resistance to a pathogen is only observed when the pathogen carries a specific avirulence gene and the plant carries a corresponding or complementing resistance gene. Hence, there is a specificity requirement to bring about enhanced disease resistance using the avr::R gene-for-gene hypersensitive response.
Many environmental and genetic factors cause general leaf necrosis in maize and other plants. In addition, numerous recessive and dominant genes cause the formation of discrete or expanding necrotic lesions of varying size, shape, and color (see, for example, Wolter et al. (1993) Mol. Gen. Genet. 239:122; Dietrich et al. (1994) Cell 77:565; Greenberg et al. (1994) Cell 77:551). Because lesions of some of these mutants resemble those associated with known diseases of maize, these genetic defects have been collectively called disease lesion mimics.
Lesion mimic mutations of maize have been shown to be specified by more than forty independent loci. It is intriguing that more than two thirds of these disease lesion mimic mutations display a partially dominant, gain-of-function inheritance, making it the largest class of dominant mutants in maize. These lesion mimic plants produce discrete disease-like symptoms in the absence of any invading pathogens.
Despite the availability of the large number of lesion mimic mutations in plants, the mechanistic basis and significance of this phenomenon, and the wild-type function of the genes involved, are poorly understood. The expression of most, if not all, lesion mimics is developmentally programmed and is easily affected by genetic background. One nearly ubiquitous feature of most mimics is the death of afflicted tissues, the extent of which is often enhanced by intense light, making it likely that reactive oxygen species are involved in the etiology of lesion mimics (see, for example, Johal et al. (1995) BioEssays 17:685; Dangl et al. (1996) Plant Cell 8:1793). In fact, superoxide has been shown to be responsible for the expression of lesions in the Arabidopsis lsd1 mutant (Jabs et al. (1996) Science 273:1853). The existence of both determinant and propagative lesion type mimics suggests that cell death is either initiated precociously or is contained inadequately in these mutants. Since cell death in plants, like in animals, has relevance to development, differentiation, and maintenance, lesion mimics afford an excellent model for understanding how cell death is regulated and executed in plants. Recently, genes for three mimics from three plant species have been cloned (Buschges et al. (1997) Cell 88:695-705; Dietrich et al. (1997) Cell 88:685-694; Gray et al. (1997) Cell 89:25-31). As expected from their recessive loss-of-function phenotypes, they all appear to encode cell death suppressible functions that are unique to plants.
While it is relatively straightforward to comprehend the nature of the defect in a recessive loss-of-function mutation, it is often not possible to predict from the phenotype what the mechanistic basis of a dominant mutation might be. One such maize dominant mutation is Les22 (previously designated Les*-2552), which is characterized by the formation of discrete, tiny whitish gray bleached or necrotic spots on leaf blades that partly resemble hypersensitive response lesions in appearance. Like most lesion mimics of maize, the expression of Les22 lesions is cell autonomous, developmentally dictated, and light-dependent.
Cell death and lesion formation during the expression of disease mutant mimics is frequently mediated by oxygen free radicals, which also mediate cell death and lesion formation during the hypersensitive response associated with gene-for-gene specificity of plant-pathogen interactions. The molecular basis for this similarity can be used to genetically engineer plants for enhanced disease resistance.